Proliferation and death of oligodendrocytes and myelin proteins are differentially regulated in male and female rodents

Journal of Neuroscience

Volumn 26, Issue 5, 2006, Pages 1439-1447

  Cerghet, Mirela ^a,b   Skoff, Robert P ^b   Bessert, Denise ^b   Zhang, Zhan ^b   Mullins, Chadwick ^b   Ghandour, M Said ^c  

^a HENRY FORD HOSPITAL   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CNRS   (France)

Author keywords

Apoptosis; Estradiol; Estrogen; Myelin; Oligodendrocyte; Proliferation; Sexual dimorphism

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; ANDROGEN; CALPAIN; CARBONATE DEHYDRATASE II; MYELIN PROTEIN; PROTEOLIPID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FORNIX; CASTRATION; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; CORPUS CALLOSUM; FEMALE; GLIA CELL; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; LIFESPAN; MALE; MULTIPLE SCLEROSIS; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN SYNTHESIS REGULATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SEX DIFFERENCE; SPINAL CORD; TRANSCRIPTION INITIATION; TRANSLATION INITIATION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CARBONIC ANHYDRASE II; CELL PROLIFERATION; CORPUS CALLOSUM; FEMALE; FORNIX (BRAIN); GENE EXPRESSION REGULATION; MALE; MICE; MYELIN BASIC PROTEINS; MYELIN PROTEINS; MYELIN PROTEOLIPID PROTEIN; OLIGODENDROGLIA; RATS; SEX CHARACTERISTICS; SPINAL CORD;

EID: 32544454801     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2219-05.2006     Document Type: Article

References (52)

1. Alonso G (2000) Prolonged corticosterone treatment of adult rats inhibits the proliferation of oligodendrocyte progenitors present throughout white and gray matter regions of the brain. Glia 31:219-231.
2. Andrade JP, Madeira MD, Paula-Barbosa MM (2000) Sexual dimorphism in the subiculum of the rat hippocampal formation. Brain Res 875:125-137.
3. Bansal R, Stefansson K, Pfeiffer SE (1992) Proligodendroblast antigen (POA), a developmental antigen expressed by AOO7/O4-positive oligodendrocyte progenitors prior to the appearance of sulfatide and galactocerebroside. J Neurochem 58:2221-2229.
4. Barrera A, Jimenez L, Gonzalez GM, Montiel J, Aboitiz F (2001) Dendritic structure of single hippocampal neurons according to sex and hemisphere of origin in middle-aged and elderly human subjects. Brain Res 906:31-37.
5. Bebo Jr BF, Vandenbark AA, Offner H (1996) Male SJL mice do not relapse after induction of EAE with PLP 139-151. J Neurosci Res 45:680-689.
6. Benjamins JA, Morell P (1978) Proteins of myelin and their metabolism. Neurochem Res 3:137-174.
7. Berrebi AS, Fitch RH, Ralphe DL, Denenberg JO, Friedrich Jr VL, Denenberg VH (1988) Corpus callosum: region-specific effects of sex, early experience and age. Brain Res 438:216-224.
8. Bessert DA, Skoff RP (1999) High-resolution in situ hybridization and TUNEL staining with free-floating brain sections. J Histochem Cytochem 47:693-702.
9. Bimonte HA, Fitch RH, Denenberg VH (2000) Neonatal estrogen blockade prevents normal callosal responsiveness to estradiol in adulthood. Brain Res Dev Brain Res 122:149-155.
10. Cerghet M, Bessert DA, Nave KA, Skoff RP (2001) Differential expression of apoptotic markers in jimpy and in Plp overexpressors: evidence for different apoptotic pathways. J Neurocytol 30:841-855.
11. Daston G, Lamar E, Olivier M, Goulding M (1996) pax-3 is necessary for migration but not differentiation of limb muscle precursors in the mouse. Development 122:1017-1027.
12. Finley SK, Kritzer MF (1999) Immunoreactivity for intracellular androgen receptors in identified subpopulations of neurons, astrocytes and oligodendrocytes in primate prefrontal cortex. J Neurobiol 40:446-457.
13. Fitch RH, Berrebi AS, Cowell PE, Schrott LM, Denenberg VH (1990) Corpus callosum: effects of neonatal hormones on sexual dimorphism in the rat. Brain Res 51:111-116.
14. Garcia-Segura LM, Chowen JA, Parducz A, Naftolin F (1994) Gonadal steroids as promoters of neuro-glial plasticity. Prog Neurobiol 4:279-307.
15. Ghandour MS, Skoff RP (1991) Double-labeling in situ hybridization analysis of mRNAs for carbonic anhydrase II and myelin basic protein: expression in developing cultured glial cells. Glia 4:1-10.
16. Ghandour MS, Langley OK, Vincendon G, Gombos G (1979) Double labeling immunohistochemical technique provides evidence of the specificity of glial cell markers. J Histochem Cytochem 27:1634-1637.
17. Goldstein JM, Seidman LJ, Horton NJ, Makris N, Kennedy DN, Caviness Jr VS, Faraone SV, Tsuang MT (2001) Normal sexual dimorphism of the adult brain assessed by in vivo magnetic resonance imaging. Cereb Cortex 11:490-497.
18. Guillery RW, Herrup K (1997) Quantification without pontification: choosing a method for counting objects in sectioned tissues. J Comp Neurol 386:2-7.
19. Gur RC, Turetsky BI, Matsui M, Yan M, Bilker W, Hughett P, Gur RE (1999) Sex differences in brain gray and white matter in healthy young adults: correlations with cognitive performance. J Neurosci 19:4065-4072.
20. Harasty J, Double KL, Halliday GM, Kril JJ, McRitchie DA (1997) Language-associated cortical regions are proportionally larger in the female brain. Arch Neurol 54:171-176.
21. Jacobson CD, Gorski RA (1981) Neurogenesis of the sexually dimorphic nucleus of the preoptic area in the rat. J Comp Neurol 196:519-529.
22. Jalabi W, Cerghet M, Skoff RP, Ghandour MS (2003) Detection of oligodendrocytes in tissue sections using PCR synthesis of digoxigenin-labeled probes. J Histochem Cytochem 51:913-919.
23. Jung-Testas I, Renoir JM, Gase JM, Baulieu EE (1991) Estrogen-inducible progesterone receptor in primary cultures of rat glial cells. Exp Cell Res 193:12-19.
24. Jung-Testas I, Schumacher M, Robel P, Baulieu EE (1994) Actions of steroid hormones and growth factors on glial cells of the central and peripheral nervous system. J Steroid Biochem Mol Biol 48:145-154.
25. Kim JH, Juraska JM (1997) Sex differences in the development of axon number in the splenium of the rat corpus callosum from postnatal day 15 through 60. Brain Res Dev Brain Res 102:77-85.
26. Knapp PE, Dutta S, Skoff RP (1990) Differences in levels of neuroglial cell death in jimpy male mice and carrier females. Dev Neurosci 12:145-152.
27. Knapp PE, Benjamins JA, Skoff RP (1996) Epigenetic factors up-regulate expression of myelin proteins in the dysmyelinating jimpy mutant mouse. J Neurobiol 29:138-150.
28. Korr H, Schultze B, Maurer W (1973) Autoradiographic investigations of glial proliferation in the brain of adult mice. I. The DNA synthesis phase of neuroglia and endothelial cells. J Comp Neurol 150:169-176.
29. Mack CM, Boehm GW, Berrebi AS, Denenberg VH (1995) Sex differences in the distribution of axon types within the genu of the rat corpus callosum. Brain Res 697:152-160.
30. Marin-Husstege M, Muggironi M, Raban D, Skoff RP, Casaccia-Bonnefil P (2004) Oligodendrocyte progenitor proliferation and maturation is differentially regulated by male and female sex steroid hormones. Dev Neurosci 26:245-254.
31. Markowska AL (1999) Sex dimorphisms in the rate of age-related decline in spatial memory: relevance to alterations in the estrous cycle. J Neurosci 19:8122-8133.
32. Mong JA, Kurzweil RL, Davis AM, Rocca MS, McCarthy MM (1996) Evidence for sexual differentiation of glia in rat brain. Horm Behav 30:553-562.
33. Mong JA, Glaser E, McCarthy MM (1999) Gonadal steroids promote glial differentiation and alter neuronal morphology in the developing hypothalamus in a regional specific manner. J Neurosci 19:1464-1472.
34. Moscarello MA, Wood DD, Ackerley C, Boulias C (1994) Myelin in multiple sclerosis is developmentally immature. J Clin Invest 94:146-154.
35. Nave KA, Bloom FE, Milner RJ (1987) A single nucleotide difference in the gene for myelin proteolipid protein defines the jimpy mutation in mouse. J Neurochem 49:1873-1877.
36. Nottebohm F, Arnold AP (1976) Sexual dimorphism in vocal control areas of the songbird brain. Science 194:211-213.
37. Nuñez JL, Nelson J, Pych JC, Kim JHY, Juraska JM (2000) Myelination in the splenium of the corpus callosum in adult male and female rats. Dev Brain Res 120:87-90.
38. Quadros PS, Lopez V, De Vries GJ, Chung WC, Wagner CK (2002) Progesterone receptors and the sexual differentiation of the medial preoptic nucleus. J Neurobiol 51:24-32.
39. Ray SK, Shields DC, Saido TC, Matzelle DC, Wilford GG, Hogan EL, Banik NL (1999) Calpain activity and translational expression increased in spinal cord injury. Brain Res 816:375-380.
40. Roof RL (1993) Neonatal exogenous testosterone modifies sex difference in radial arm and Morris water maze performance in prepubescent and adult rats. Behav Brain Res 53:1-10.
41. Schaecher K, Rocchini A, Dinkins J, Matzelle DD, Banik NL (2002) Calpain expression and infiltration of activated cells in experimental allergic encephalomyelitis over time: increased calpain activity begins with onset of disease. J Neuroimmunol 129:1-9.
42. Schlaepfer TE, Harris GJ, Tien AY, Peng L, Lee S, Pearlson GD (1995) Structural differences in the cerebral cortex of healthy female and male subjects: a magnetic resonance imaging study. Psychiatry Res 61:129-135.
43. Sherry DF, Jacobs LF, Gaulin SJ (1992) Spatial memory and adaptive specialization of the hippocampus. Trends Neurosci 15:56-57.
44. Shields DC, Schaecher KE, Saido TC, Banik NL (1999) A putative mechanism of demyelination in multiple sclerosis by a proteolitic enzyme, calpain. Proc Natl Acad Sci USA 96:11486-11491.
45. Sorg BA, Smith MM, Campagnoni AT (1987) Developmental expression of the myelin proteolipid protein and basic protein mRNAs in normal and dysmyelinating mutant mice. J Neurochem 49:1146-1154.
46. Staugaitis SM, Smith PR, Colman DR (1990) Expression of myelin basic protein isoforms in nonglial cells. J Cell Biol 110:1719-1727.
47. Sturrock RR (1981) Electron microscopic evidence for mitotic division of oligodendrocytes. J Anat 132:429-432.
48. Takao T, Flint N, Lee L, Ying X, Merrill J, Chandross KJ (2004) 17 Betae-stradiol protects oligodendrocytes from cytotoxicity induced cell death. J Neurochem 89:660-673.
49. Tomassini V, Onesti E, Mainero C, Giugni E, Paolillo A, Salvetti M, Nicolettit F, Pozzilli C (2005) Sex hormones modulate brain damage in multiple sclerosis: MRI evidence. J Neurol Neurosurg Psychiatry 76:272-275.
50. Voskuhl RR, Palaszynski K (2001) Sex hormones in experimental autoimmune encephalomyelitis: implications for multiple sclerosis. The Neuroscientist 7:258-270.
51. Zhang Z, Cerghet M, Mullins C, Williamson M, Bessert D, Skoff R (2004) Comparison of in vivo and in vitro subcellular localization of estrogen receptors alpha and beta in oligodendrocytes. J Neurochem 89:674-684.
52. Zwain IH, Yen SS (1999) Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 140:3843-3852.